Top

BMC Medicine

Published in:

Open Access 01-12-2013 | Research article

How do autoimmune diseases cluster in families? A systematic review and meta-analysis

Authors: Jorge Cárdenas-Roldán, Adriana Rojas-Villarraga, Juan-Manuel Anaya

Published in: BMC Medicine | Issue 1/2013

Abstract

Background

A primary characteristic of complex genetic diseases is that affected individuals tend to cluster in families (that is, familial aggregation). Aggregation of the same autoimmune condition, also referred to as familial autoimmune disease, has been extensively evaluated. However, aggregation of diverse autoimmune diseases, also known as familial autoimmunity, has been overlooked. Therefore, a systematic review and meta-analysis were performed aimed at gathering evidence about this topic.

Methods

Familial autoimmunity was investigated in five major autoimmune diseases, namely, rheumatoid arthritis, systemic lupus erythematosus, autoimmune thyroid disease, multiple sclerosis and type 1 diabetes mellitus. Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines were followed. Articles were searched in Pubmed and Embase databases.

Results

Out of a total of 61 articles, 44 were selected for final analysis. Familial autoimmunity was found in all the autoimmune diseases investigated. Aggregation of autoimmune thyroid disease, followed by systemic lupus erythematosus and rheumatoid arthritis, was the most encountered.

Conclusions

Familial autoimmunity is a frequently seen condition. Further study of familial autoimmunity will help to decipher the common mechanisms of autoimmunity.

Available only for authorised users

Anaya JM, Shoenfeld Y, Correa PA, García-Carrasco M, Cervera R: Autoinmunidad y Enfermedad Autoinmune. 2005, Medellín: CIB

Cooper GS, Stroehla BC: The epidemiology of autoimmune diseases. Autoimmun Rev. 2003, 2: 119-125. 10.1016/S1568-9972(03)00006-5.PubMed

Youinou P, Pers JO, Gershwin ME, Shoenfeld Y: Geo-epidemiology and autoimmunity. J Autoimmun. 2010, 34: J163-167. 10.1016/j.jaut.2009.12.005.PubMed

Cho JH, Gregersen PK: Genomics and the multifactorial nature of human autoimmune disease. N Engl J Med. 2011, 365: 1612-1623. 10.1056/NEJMra1100030.PubMed

Tobon GJ, Pers JO, Canas CA, Rojas-Villarraga A, Youinou P, Anaya JM: Are autoimmune diseases predictable?. Autoimmun Rev. 2012, 11: 259-266. 10.1016/j.autrev.2011.10.004.PubMed

Anaya JM: The autoimmune tautology. Arthritis Res Ther. 2010, 12: 147-10.1186/ar3175.PubMedPubMedCentral

Anaya JM: Common mechanisms of autoimmune diseases (the autoimmune tautology). Autoimmun Rev. 2012, 11: 781-784. 10.1016/j.autrev.2012.02.002.PubMed

Rojas-Villarraga A, Amaya-Amaya J, Rodriguez-Rodriguez A, Mantilla RD, Anaya JM: Introducing polyautoimmunity: secondary autoimmune diseases no longer exist. Autoimmune Dis. 2012, 2012: 254319.PubMedPubMedCentral

Anaya JM, Corena R, Castiblanco J, Rojas-Villarraga A, Shoenfeld Y: The kaleidoscope of autoimmunity: multiple autoimmune syndromes and familial autoimmunity. Expert Rev Clin Immunol. 2007, 3: 623-635. 10.1586/1744666X.3.4.623.PubMed

10.

Castiblanco J, Anaya JM: The nature and nurture of common autoimmunity. Ann N Y Acad Sci. 2007, 1109: 1-8. 10.1196/annals.1398.001.PubMed

11.

Lorber M, Gershwin ME, Shoenfeld Y: The coexistence of systemic lupus erythematosus with other autoimmune diseases: the kaleidoscope of autoimmunity. Semin Arthritis Rheum. 1994, 24: 105-113. 10.1016/S0049-0172(05)80004-6.PubMed

12.

Shoenfeld Y: The kaleidoscope of autoimmunity. Autoimmunity. 1993, 15: 245-252. 10.3109/08916939309019934.PubMed

13.

Sloka S: Observations on recent studies showing increased co-occurrence of autoimmune diseases. J Autoimmun. 2002, 18: 251-257. 10.1006/jaut.2002.0588.PubMed

14.

Weiss P, Shoenfeld Y: Shifts in autoimmune diseases: the kaleidoscope of autoimmunity. Isr J Med Sci. 1991, 27: 215-217.PubMed

15.

Humbert P, Dupond JL: Multiple autoimmune syndromes (French). Ann Med Interne (Paris). 1988, 139: 159-168.

16.

Anaya JM, Castiblanco J, Rojas-Villarraga A, Pineda-Tamayo R, Levy RA, Gomez-Puerta J, Dias C, Mantilla RD, Gallo JE, Cervera R, Shoenfeld Y, Arcos-Burgos M: The multiple autoimmune syndromes. A clue for the autoimmune tautology. Clin Rev Allergy Immunol. 2012, 43: 256-264. 10.1007/s12016-012-8317-z.PubMed

17.

Eisenbarth GS, Gottlieb PA: Autoimmune polyendocrine syndromes. N Engl J Med. 2004, 350: 2068-2079. 10.1056/NEJMra030158.PubMed

18.

Quintero OL, Amador-Patarroyo MJ, Montoya-Ortiz G, Rojas-Villarraga A, Anaya JM: Autoimmune disease and gender: plausible mechanisms for the female predominance of autoimmunity. J Autoimmun. 2012, 38: J109-119. 10.1016/j.jaut.2011.10.003.PubMed

19.

Cruz-Tapias P, Perez-Fernandez OM, Rojas-Villarraga A, Rodriguez-Rodriguez A, Arango MT, Anaya JM: Shared HLA class II in six autoimmune diseases in Latin America: A meta-analysis. Autoimmune Dis. 2012, 2012: 569728.PubMedPubMedCentral

20.

Barragan-Martinez C, Speck-Hernandez CA, Montoya-Ortiz G, Mantilla RD, Anaya JM, Rojas-Villarraga A: Organic solvents as risk factor for autoimmune diseases: a systematic review and meta-analysis. PLoS One. 2012, 7: e51506-10.1371/journal.pone.0051506.PubMedPubMedCentral

21.

George J, Levy Y, Shoenfeld Y: Smoking and immunity: an additional player in the mosaic of autoimmunity. Scand J Immunol. 1997, 45: 1-6. 10.1046/j.1365-3083.1997.d01-366.x.PubMed

22.

Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Harley JB: Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003, 349: 1526-1533. 10.1056/NEJMoa021933.PubMed

23.

Scofield RH: Autoantibodies as predictors of disease. Lancet. 2004, 363: 1544-1546. 10.1016/S0140-6736(04)16154-0.PubMed

24.

Harel M, Shoenfeld Y: Predicting and preventing autoimmunity, myth or reality?. Ann N Y Acad Sci. 2006, 1069: 322-345. 10.1196/annals.1351.031.PubMed

25.

Shepshelovich D, Shoenfeld Y: Prediction and prevention of autoimmune diseases: additional aspects of the mosaic of autoimmunity. Lupus. 2006, 15: 183-190. 10.1191/0961203306lu2274rr.PubMed

26.

Sherer Y, Shoenfeld Y: Antiphospholipid antibodies: are they pro-atherogenic or an epiphenomenon of atherosclerosis?. Immunobiology. 2003, 207: 13-16. 10.1078/0171-2985-00212.PubMed

27.

Shoenfeld Y: Primary biliary cirrhosis and autoimmune rheumatic diseases: prediction and prevention. Isr J Med Sci. 1992, 28: 113-116.PubMed

28.

OCEBM Levels of Evidence Working Group*: "The Oxford 2011 levels of evidence". Oxford Centre for Evidence-Based Medicine. [http://www.cebm.net/index.aspx?o%20=%205653]

29.

Madani S, Shapiro J: Alopecia areata update. J Am Acad Dermatol. 2000, 42: 549-566.PubMed

30.

Cotch MF, Hoffman GS, Yerg DE, Kaufman GI, Targonski P, Kaslow RA: The epidemiology of Wegener's granulomatosis. Estimates of the five-year period prevalence, annual mortality, and geographic disease distribution from population-based data sources. Arthritis Rheum. 1996, 39: 87-92. 10.1002/art.1780390112.PubMed

31.

Jacobson DL, Gange SJ, Rose NR, Graham NM: Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol. 1997, 84: 223-243. 10.1006/clin.1997.4412.PubMed

32.

Barcellos LF, Kamdar BB, Ramsay PP, DeLoa C, Lincoln RR, Caillier S, Schmidt S, Haines JL, Pericak-Vance MA, Oksenberg JR, Hauser SL: Clustering of autoimmune diseases in families with a high-risk for multiple sclerosis: a descriptive study. Lancet Neurol. 2006, 5: 924-931. 10.1016/S1474-4422(06)70552-X.PubMed

33.

Boelaert K, Newby PR, Simmonds MJ, Holder RL, Carr-Smith JD, Heward JM, Manji N, Allahabadia A, Armitage M, Chatterjee KV, Lazarus JH, Pearce SH, Vaidya B, Gough SC, Franklyn JA: Prevalence and relative risk of other autoimmune diseases in subjects with autoimmune thyroid disease. Am J Med. 2010, 123: 183.PubMed

34.

Hemminki K, Li X, Sundquist J, Sundquist K: The epidemiology of Graves' disease: evidence of a genetic and an environmental contribution. J Autoimmun. 2010, 34: J307-J313. 10.1016/j.jaut.2009.11.019.PubMed

35.

Criswell LA, Pfeiffer KA, Lum RF, Gonzales B, Novitzke J, Kern M, Moser KL, Begovich AB, Carlton VE, Li W, Lee AT, Ortmann W, Behrens TW, Gregersen PK: Analysis of families in the multiple autoimmune disease genetics consortium (MADGC) collection: the PTPN22 620W allele associates with multiple autoimmune phenotypes. Am J Hum Genet. 2005, 76: 561-571. 10.1086/429096.PubMedPubMedCentral

36.

Bottazzo GF, Mann JI, Thorogood M: Autoimmunity in juvenile diabetics and their families. BMJ. 1978, 2: 165-168. 10.1136/bmj.2.6131.165.PubMedPubMedCentral

37.

Anaya JM, Castiblanco J, Tobon GJ, Garcia J, Abad V, Cuervo H, Velasquez A, Angel ID, Vega P, Arango A: Familial clustering of autoimmune diseases in patients with type 1 diabetes mellitus. J Autoimmun. 2006, 26: 208-214. 10.1016/j.jaut.2006.01.001.PubMed

38.

Wagner AM, Santana A, Hernndez M, Wiebe JC, Novoa J, Mauricio D: Predictors of associated autoimmune diseases in families with type 1 diabetes: results from the Type 1 Diabetes Genetics Consortium. Diabetes Metab Res Rev. 2011, 27: 493-498. 10.1002/dmrr.1189.PubMedPubMedCentral

39.

Hemminki K, Li X, Sundquist J, Sundquist K: Familial association between type 1 diabetes and other autoimmune and related diseases. Diabetologia. 2009, 52: 1820-1828. 10.1007/s00125-009-1427-3.PubMed

40.

Samuelsson U, Sadauskaite V, Padaiga Z, Ludvigsson J: A fourfold difference in the incidence of type 1 diabetes between Sweden and Lithuania but similar prevalence of autoimmunity. Diabetes Res Clin Pract. 2004, 66: 173-181. 10.1016/j.diabres.2004.03.001.PubMed

41.

Lebenthal Y, Yackobovitch-Gavan M, de Vries L, Phillip M, Lazar L: Coexistent autoimmunity in familial type 1 diabetes: increased susceptibility in sib-pairs?. Horm Res Paediatr. 2011, 75: 284-290. 10.1159/000322936.PubMedPubMedCentral

42.

Alarcon-Segovia D, Alarcon-Riquelme ME, Cardiel MH, Caeiro F, Massardo L, Villa AR, Pons-Estel BA: Familial aggregation of systemic lupus erythematosus, rheumatoid arthritis, and other autoimmune diseases in 1,177 lupus patients from the GLADEL cohort. Arthritis Rheum. 2005, 52: 1138-1147. 10.1002/art.20999.PubMed

43.

Priori R, Medda E, Conti F, Cassara EAM, Danieli MG, Gerli R, Giacomelli R, Franceschini F, Manfredi A, Pietrogrande M, Stazi MA, Valesini G: Familial autoimmunity as a risk factor for systemic lupus erythematosus and vice versa: a case-control study. Lupus. 2003, 12: 735-740. 10.1191/0961203303lu457oa.PubMed

44.

Corporaal S, Bijl M, Kallenberg CG: Familial occurrence of autoimmune diseases and autoantibodies in a Caucasian population of patients with systemic lupus erythematosus. Clin Rheumatol. 2002, 21: 108-113. 10.1007/PL00011215.PubMed

45.

Lin JP, Cash JM, Doyle SZ, Peden S, Kanik K, Amos CI, Bale SJ, Wilder RL: Familial clustering of rheumatoid arthritis with other autoimmune diseases. Hum Genet. 1998, 103: 475-482. 10.1007/s004390050853.PubMed

46.

Thomas DJ, Young A, Gorsuch AN, Bottazzo GF, Cudworth AG: Evidence for an association between rheumatoid arthritis and autoimmune endocrine disease. Ann Rheum Dis. 1983, 42: 297-300. 10.1136/ard.42.3.297.PubMedPubMedCentral

47.

Hemminki K, Li X, Sundquist J, Sundquist K: Familial associations of rheumatoid arthritis with autoimmune diseases and related conditions. Arthritis Rheum. 2009, 60: 661-668. 10.1002/art.24328.PubMed

48.

Jawaheer D, Lum RF, Amos CI, Gregersen PK, Criswell LA: Clustering of disease features within 512 multicase rheumatoid arthritis families. Arthritis Rheum. 2004, 50: 736-741. 10.1002/art.20066.PubMed

49.

Broadley SA, Deans J, Sawcer SJ, Clayton D, Compston DA: Autoimmune disease in first-degree relatives of patients with multiple sclerosis. A UK survey. Brain. 2000, 123: 1102-1111. 10.1093/brain/123.6.1102.PubMed

50.

Deretzi G, Kountouras J, Koutlas E, Zavos C, Polyzos S, Rudolf J, Grigoriadis N, Gavalas E, Boziki M, Tsiptsios I: Familial prevalence of autoimmune disorders in multiple sclerosis in Northern Greece. Mult Scler. 2010, 16: 1091-1101. 10.1177/1352458510375708.PubMed

51.

Heinzlef O, Alamowitch S, Sazdovitch V, Chillet P, Joutel A, Tournier-Lasserve E, Roullet E: Autoimmune diseases in families of French patients with multiple sclerosis. Acta Neurol Scand. 2000, 101: 36-40. 10.1034/j.1600-0404.2000.101001036.x.PubMed

52.

Henderson RD, Bain CJ, Pender MP: The occurrence of autoimmune diseases in patients with multiple sclerosis and their families. J Clin Neurosci. 2000, 7: 434-437. 10.1054/jocn.2000.0693.PubMed

53.

Marrosu MG, Cocco E, Lai M, Spinicci G, Pischedda MP, Contu P: Patients with multiple sclerosis and risk of type 1 diabetes mellitus in Sardinia, Italy: a cohort study. Lancet. 2002, 359: 1461-1465. 10.1016/S0140-6736(02)08431-3.PubMed

54.

Ramagopalan SV, Dyment DA, Valdar W, Herrera BM, Criscuoli M, Yee IM, Sadovnick AD, Ebers GC: Autoimmune disease in families with multiple sclerosis: a population-based study. Lancet Neurol. 2007, 6: 604-610. 10.1016/S1474-4422(07)70132-1.PubMed

55.

Nielsen NM, Frisch M, Rostgaard K, Wohlfahrt J, Hjalgrim H, Koch-Henriksen N, Melbye M, Westergaard T: Autoimmune diseases in patients with multiple sclerosis and their first-degree relatives: a nationwide cohort study in Denmark. Mult Scler. 2008, 14: 823-829. 10.1177/1352458508088936.PubMed

56.

Laroni A, Calabrese M, Perini P, Albergoni MP, Ranzato F, Tiberio M, Battistin L, Gallo P: Multiple sclerosis and autoimmune diseases: epidemiology and HLA-DR association in North-east Italy. J Neurol. 2006, 253: 636-639. 10.1007/s00415-006-0084-4.PubMed

57.

Arora-Singh RK, Assassi S, del Junco DJ, Arnett FC, Perry M, Irfan U, Sharif R, Mattar T, Mayes MD: Autoimmune diseases and autoantibodies in the first degree relatives of patients with systemic sclerosis. J Autoimmun. 2010, 35: 52-57. 10.1016/j.jaut.2010.02.001.PubMedPubMedCentral

58.

Hudson M, Rojas-Villarraga A, Coral-Alvarado P, Lopez-Guzman S, Mantilla RD, Chalem P, Baron M, Anaya JM: Polyautoimmunity and familial autoimmunity in systemic sclerosis. J Autoimmun. 2008, 31: 156-159. 10.1016/j.jaut.2008.05.002.PubMed

59.

Koumakis E, Dieudé P, Avouac J, Kahan A, Allanore Y: Familial autoimmunity in systemic sclerosis - Results of a French-based case-control family study. J Rheumatol. 2012, 39: 532-538. 10.3899/jrheum.111104.PubMed

60.

Frech T, Khanna D, Markewitz B, Mineau G, Pimentel R, Sawitzke A: Heritability of vasculopathy, autoimmune disease, and fibrosis in systemic sclerosis: a population-based study. Arthritis Rheum. 2010, 62: 2109-2116.PubMedPubMedCentral

61.

Reveille JD, Wilson RW, Provost TT, Bias WB, Arnett FC: Primary Sjogren's syndrome and other autoimmune diseases in families. Prevalence and immunogenetic studies in six kindreds. Ann Intern Med. 1984, 101: 748-756.PubMed

62.

Anaya JM, Tobon GJ, Vega P, Castiblanco J: Autoimmune disease aggregation in families with primary Sjogren's syndrome. J Rheumatol. 2006, 33: 2227-2234.PubMed

63.

Hemminki K, Li X, Sundquist K, Sundquist J: Familial association of inflammatory bowel diseases with other autoimmune and related diseases. Am J Gastroenterol. 2010, 105: 139-147. 10.1038/ajg.2009.496.PubMed

64.

Alkhateeb A, Fain PR, Thody A, Bennett DC, Spritz RA: Epidemiology of vitiligo and associated autoimmune diseases in Caucasian probands and their families. Pigment Cell Res. 2003, 16: 208-214. 10.1034/j.1600-0749.2003.00032.x.PubMed

65.

Laberge G, Mailloux CM, Gowan K, Holland P, Bennett DC, Fain PR, Spritz RA: Early disease onset and increased risk of other autoimmune diseases in familial generalized vitiligo. Pigment Cell Res. 2005, 18: 300-305. 10.1111/j.1600-0749.2005.00242.x.PubMed

66.

Zhang Z, Xu SX, Zhang FY, Yin XY, Yang S, Xiao FL, Du WH, Wang JF, Lv YM, Tang HY, Zhang XJ: The analysis of genetics and associated autoimmune diseases in Chinese vitiligo patients. Arch Dermatol Res. 2009, 301: 167-173. 10.1007/s00403-008-0900-z.PubMed

67.

Prahalad S, Shear ES, Thompson SD, Giannini EH, Glass DN: Increased prevalence of familial autoimmunity in simplex and multiplex families with juvenile rheumatoid arthritis. Arthritis Rheum. 2002, 46: 1851-1856. 10.1002/art.10370.PubMed

68.

Huang CM, Yang YH, Chiang BL: Different familial association patterns of autoimmune diseases between juvenile-onset systemic lupus erythematosus and juvenile rheumatoid arthritis. J Microbiol Immunol Infect. 2004, 37: 88-94.PubMed

69.

Walters HM, Pan N, Moorthy LN, Ward MJ, Peterson MG, Lehman TJ: Patterns and influence of familial autoimmunity in pediatric systemic lupus erythematosus. Pediatr Rheumatol Online J. 2012, 10: 22-10.1186/1546-0096-10-22.PubMedPubMedCentral

70.

Ginn LR, Lin JP, Plotz PH, Bale SJ, Wilder RL, Mbauya A, Miller FW: Familial autoimmunity in pedigrees of idiopathic inflammatory myopathy patients suggests common genetic risk factors for many autoimmune diseases. Arthritis Rheum. 1998, 41: 400-405. 10.1002/1529-0131(199803)41:3<400::AID-ART4>3.0.CO;2-5.PubMed

71.

Niewold TB, Wu SC, Smith M, Morgan GA, Pachman LM: Familial aggregation of autoimmune disease in juvenile dermatomyositis. Pediatrics. 2011, 127: e1239-1246. 10.1542/peds.2010-3022.PubMedPubMedCentral

72.

Petaros P, Martelossi S, Tommasini A, Torre G, Caradonna M, Ventura A: Prevalence of autoimmune disorders in relatives of patients with celiac disease. Dig Dis Sci. 2002, 47: 1427-1431. 10.1023/A:1015830110836.PubMed

73.

Cataldo F, Marino V: Increased prevalence of autoimmune diseases in first-degree relatives of patients with celiac disease. J Pediatr Gastroenterol Nutr. 2003, 36: 470-473. 10.1097/00005176-200304000-00009.PubMed

74.

Neuhausen SL, Steele L, Ryan S, Mousavi M, Pinto M, Osann KE, Flodman P, Zone JJ: Co-occurrence of celiac disease and other autoimmune diseases in celiacs and their first-degree relatives. J Autoimmun. 2008, 31: 160-165. 10.1016/j.jaut.2008.06.001.PubMedPubMedCentral

75.

Kakourou T, Karachristou K, Chrousos G: A case series of alopecia areata in children: impact of personal and family history of stress and autoimmunity. J Eur Acad Dermatol Venereol. 2007, 21: 356-359. 10.1111/j.1468-3083.2006.01931.x.PubMed

76.

Pérez-Fernández OM, Mantilla RD, Cruz-Tapias P, Rodriguez-Rodriguez A, Rojas-Villarraga A, Anaya J-M: Spondyloarthropathies in autoimmune diseases and vice versa. Autoimmune Dis. 2012, 2012: 736384.PubMedPubMedCentral

77.

Roberts CGP, Ladenson PW: Hypothyroidism. Lancet. 2004, 363: 793-803. 10.1016/S0140-6736(04)15696-1.PubMed

78.

Shapira Y, Agmon-Levin N, Shoenfeld Y: Defining and analyzing geoepidemiology and human autoimmunity. J Autoimmun. 2010, 34: J168-177. 10.1016/j.jaut.2009.11.018.PubMed

79.

Wiebolt J, Achterbergh R, den Boer A, van der Leij S, Marsch E, Suelmann B, de Vries R, van Haeften TW: Clustering of additional autoimmunity behaves differently in Hashimoto's patients compared with Graves' patients. Eur J Endocrinol. 2011, 164: 789-794. 10.1530/EJE-10-1172.PubMed

80.

Szyper-Kravitz M, Marai I, Shoenfeld Y: Coexistence of thyroid autoimmunity with other autoimmune diseases: friend or foe? Additional aspects on the mosaic of autoimmunity. Autoimmunity. 2005, 38: 247-255. 10.1080/08916930500050194.PubMed

81.

Dittmar M, Libich C, Brenzel T, Kahaly GJ: Increased familial clustering of autoimmune thyroid diseases. Horm Metab Res. 2011, 43: 200-204. 10.1055/s-0031-1271619.PubMed

82.

Scofield RH, Bruner GR, Harley JB, Namjou B: Autoimmune thyroid disease is associated with a diagnosis of secondary Sjogren's syndrome in familial systemic lupus. Ann Rheum Dis. 2007, 66: 410-413. 10.1136/ard.2006.055103.PubMed

83.

Taneja V, Singh RR, Malaviya AN, Anand C, Mehra NK: Occurrence of autoimmune diseases and relationship of autoantibody expression with HLA phenotypes in multicase rheumatoid arthritis families. Scand J Rheumatol. 1993, 22: 152-157. 10.3109/03009749309099263.PubMed

84.

Walker DJ, Griffiths M, Griffiths ID: Occurrence of autoimmune diseases and autoantibodies in multicase rheumatoid arthritis families. Ann Rheum Dis. 1986, 45: 323-326. 10.1136/ard.45.4.323.PubMedPubMedCentral

85.

Midgard R, Gronning M, Riise T, Kvale G, Nyland H: Multiple sclerosis and chronic inflammatory diseases. A case-control study. Acta Neurol Scand. 1996, 93: 322-328.PubMed

86.

Annunziata P, Morana P, Giorgio A, Galeazzi M, Campanella V, Lore F, Guarino E: High frequency of psoriasis in relatives is associated with early onset in an Italian multiple sclerosis cohort. Acta Neurol Scand. 2003, 108: 327-331. 10.1034/j.1600-0404.2003.00158.x.PubMed

87.

Alonso A, Hernan MA, Ascherio A: Allergy, family history of autoimmune diseases, and the risk of multiple sclerosis. Acta Neurol Scand. 2008, 117: 15-20.PubMed

88.

Magana-Zamora L, Chiquete E, Campos-Gonzalez ID, Cantu-Leal R, Ibarra-Bravo O, Punzo-Bravo G, Rojas-Flores I: Risk factors and outcome of patients with multiple sclerosis from the state of Michoacan Mexico: a case-control study. Rev Mex Neuroci. 2012, 13: 78-85.

89.

Pachman LM, Hayford JR, Hochberg MC, Pallansch MA, Chung A, Daugherty CD, Athreya BH, Bowyer SL, Fink CW, Gewanter HL, Jerath R, Lang BA, Szer IS, Sinacore J, Christensen ML, Dyer AR: New-onset juvenile dermatomyositis: comparisons with a healthy cohort and children with juvenile rheumatoid arthritis. Arthritis Rheum. 1997, 40: 1526-1533. 10.1002/art.1780400822.PubMed

90.

Somers EC, Thomas SL, Smeeth L, Hall AJ: Autoimmune diseases co-occurring within individuals and within families: a systematic review. Epidemiology. 2006, 17: 202-217. 10.1097/01.ede.0000193605.93416.df.PubMed

91.

Cárdenas Roldán J, Amaya-Amaya J, Castellanos-de la Hoz J, Giraldo-Villamil J, Montoya-Ortiz G, Cruz-Tapias P, Rojas-Villarraga A, Mantilla RD, Anaya J-M: Autoimmune thyroid disease in rheumatoid arthritis: a global perspective. Arthritis. 2012, 2012: 864907.PubMedPubMedCentral

92.

Harjutsalo V, Podar T, Tuomilehto J: Cumulative incidence of type 1 diabetes in 10,168 siblings of Finnish young-onset type 1 diabetic patients. Diabetes. 2005, 54: 563-569.PubMed

93.

Brix TH, Kyvik KO, Hegedus L: A population-based study of chronic autoimmune hypothyroidism in Danish twins. J Clin Endocrinol Metab. 2000, 85: 536-539. 10.1210/jc.85.2.536.PubMed

94.

Deighton CM, Walker DJ: The familial nature of rheumatoid arthritis. Ann Rheum Dis. 1991, 50: 62-65. 10.1136/ard.50.1.62.PubMedPubMedCentral

95.

Eaton WW, Rose NR, Kalaydjian A, Pedersen MG, Mortensen PB: Epidemiology of autoimmune diseases in Denmark. J Autoimmun. 2007, 29: 1-9. 10.1016/j.jaut.2007.05.002.PubMedPubMedCentral

96.

Marrie RA: Autoimmune disease and multiple sclerosis: methods, methods, methods. Lancet Neurol. 2007, 6: 575-576. 10.1016/S1474-4422(07)70157-6.PubMed

97.

Zeft A, Shear ES, Thompson SD, Glass DN, Prahalad S: Familial autoimmunity: maternal parent-of-origin effect in juvenile idiopathic arthritis. Clin Rheumatol. 2008, 27: 241-244. 10.1007/s10067-007-0778-8.PubMed

98.

Houghton KM, Page J, Cabral DA, Petty RE, Tucker LB: Systemic lupus erythematosus in the pediatric North American Native population of British Columbia. J Rheumatol. 2006, 33: 161-163.PubMed

99.

Sanchez E, Rasmussen A, Riba L, Acevedo E, Kelly JA, Langefeld CD, Garcia-De La Torre I, Maradiaga-Cecena MA, Cardiel MH, Esquivel-Valerio JA, Rodriguez-Amado J, Moctezuma JF, Miranda P, Perandones C, Castel C, Laborde HA, Alba P, Musuruana J, Goecke A, Anaya JM, Kaufman KM, Adler A, Brown EE, Alarcon GS, Kimberly RP, Edberg JC, Criswell LA, Gilkeson GS, Niewold TB, Martin J, et al: Impact of genetic ancestry and socio-demographic status on the clinical expression of systemic lupus erythematosus in Amerindian-European populations. Arthritis Rheum. 2012, 64: 3687-3694. 10.1002/art.34650.PubMedPubMedCentral

100.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D: The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009, 62: e1-34. 10.1016/j.jclinepi.2009.06.006.PubMed

101.

Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB: Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000, 283: 2008-2012. 10.1001/jama.283.15.2008.PubMed

102.

Anaya JM, Shoenfeld Y, Cervera R: Facts and challenges for the autoimmunologist. Lessons from the second Colombian autoimmune symposium. Autoimmun Rev. 2012, 11: 249-251. 10.1016/j.autrev.2011.10.001.PubMed

103.

Anaya JM, Rojas-Villarraga A, Garcia-Carrasco M: The autoimmune tautology: from polyautoimmunity and familial autoimmunity to the autoimmune genes. Autoimmune Dis. 2012, 2012: 297193.PubMedPubMedCentral

The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1741-7015/11/73/prepub

Title: How do autoimmune diseases cluster in families? A systematic review and meta-analysis
Authors: Jorge Cárdenas-Roldán
Adriana Rojas-Villarraga
Juan-Manuel Anaya
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/1741-7015-11-73

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

How do autoimmune diseases cluster in families? A systematic review and meta-analysis

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2013

Chronic cerebrospinal venous insufficiency is not associated with cognitive impairment in multiple sclerosis

Calcium-deficiency assessment and biomarker identification by an integrated urinary metabonomics analysis

Physical comorbidities in men with mood and anxiety disorders: a population-based study

Evaluation of the acceptability and usefulness of an information website for caregivers of people with bipolar disorder

Video Q&A: molecular profiling of breast cancer

Caregivers’ understanding of dementia predicts patients’ comfort at death: a prospective observational study